Evidence for aberrant astrocyte hemichannel activity in juvenile neuronal ceroid lipofuscinosis (JNCL)

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Burkovetskaya, Maria ^a   Karpuk, Nikolay ^a   Xiong, Juan ^a   Bosch, Megan ^a   Boska, Michael D ^a   Takeuchi, Hideyuki ^b   Suzumura, Akio ^b   Kielian, Tammy ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b NAGOYA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CARBENOXOLONE; CEROID; EXCITATORY AMINO ACID TRANSPORTER; GAP JUNCTION PROTEIN; GLUTAMATE AMMONIA LIGASE; BIOLOGICAL MARKER; CARRIER PROTEIN; CHAPERONE; CLN3 PROTEIN, MOUSE; GLUTAMIC ACID; MEMBRANE PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN SLICE; CELL ACTIVITY; CELL COMMUNICATION; CELL FUNCTION; CELL INCLUSION; CLN3 GENE; CONTROLLED STUDY; DISEASE COURSE; DRUG MECHANISM; FEMALE; GAP JUNCTION; GENE; GENE LOSS; HEMICHANNEL; IN VIVO STUDY; MALE; MOUSE; NEURONAL CEROID LIPOFUSCINOSIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOGENESIS; PROTEIN EXPRESSION; TREATMENT DURATION; ANIMAL; BRAIN; DEFICIENCY; DRUG EFFECTS; GENETICS; HOMEOSTASIS; KNOCKOUT MOUSE; LYSOSOME; METABOLISM; MUTATION;

ANIMALS; ASTROCYTES; BIOLOGICAL MARKERS; BRAIN; CEROID; CONNEXINS; FEMALE; GAP JUNCTIONS; GLUTAMIC ACID; HOMEOSTASIS; LYSOSOMES; MALE; MEMBRANE GLYCOPROTEINS; MEMBRANE TRANSPORT PROTEINS; MICE; MICE, KNOCKOUT; MOLECULAR CHAPERONES; MUTATION; NEURONAL CEROID-LIPOFUSCINOSES;

EID: 84899702659     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0095023     Document Type: Article

References (94)

1. Isolation of a novel gene underlying Batten disease, CLN3. (1995) The International Batten Disease Consortium. Cell 82: 949-957.
2. Wang S (2012) Juvenile neuronal ceroid lipofuscinoses. Adv Exp Med Biol 724: 138-142.
3. Rakheja D, Narayan SB, Bennett MJ (2007) Juvenile neuronal ceroidlipofuscinosis (Batten disease): a brief review and update. Curr Mol Med 7: 603-608. (Pubitemid 47618056)
4. Staropoli JF, Haliw L, Biswas S, Garrett L, Holter SM, et al. (2012) Large-scale phenotyping of an accurate genetic mouse model of JNCL identifies novel early pathology outside the central nervous system. PLoS One 7: e38310.
5. Tyynela J, Cooper JD, Khan MN, Shemilts SJ, Haltia M (2004) Hippocampal pathology in the human neuronal ceroid-lipofuscinoses: distinct patterns of storage deposition, neurodegeneration and glial activation. Brain Pathol 14: 349-357. (Pubitemid 39524963)
6. Weimer JM, Benedict JW, Getty AL, Pontikis CC, Lim MJ, et al. (2009) Cerebellar defects in a mouse model of juvenile neuronal ceroid lipofuscinosis. Brain Res 1266: 93-107.
7. Anderson GW, Goebel HH, Simonati A (2012) Human pathology in NCL. Biochim Biophys Acta.
8. Pontikis CC, Cotman SL, MacDonald ME, Cooper JD (2005) Thalamocortical neuron loss and localized astrocytosis in the Cln3Deltaex7/8 knock-in mouse model of Batten disease. Neurobiol Dis 20: 823-836. (Pubitemid 41619358)
9. Hagopian K, Lake BD, Winchester BG, Clark JB (1995) Late-infantile Batten disease: purification of the subunit c of the mitochondrial ATP synthase from storage material. Am J Med Genet 57: 272-278.
10. Johnson DW, Speier S, Qian WH, Lane S, Cook A, et al. (1995) Role of subunit- 9 of mitochondrial ATP synthase in Batten disease. Am J Med Genet 57: 350-360.
11. Sulzer D, Mosharov E, Talloczy Z, Zucca FA, Simon JD, et al. (2008) Neuronal pigmented autophagic vacuoles: lipofuscin, neuromelanin, and ceroid as macroautophagic responses during aging and disease. J Neurochem 106: 24-36. (Pubitemid 351850210)
12. Riga D, Riga S, Halalau F, Schneider F (2006) Brain lipopigment accumulation in normal and pathological aging. Ann N Y Acad Sci 1067: 158-163. (Pubitemid 43806320)
13. Braak E, Sandmann-Keil D, Rub U, Gai WP, de Vos RA, et al. (2001) alphasynuclein immunopositive Parkinson's disease-related inclusion bodies in lower brain stem nuclei. Acta Neuropathol 101: 195-201. (Pubitemid 32219751)
14. Seehafer SS, Pearce DA (2006) You say lipofuscin, we say ceroid: defining autofluorescent storage material. Neurobiol Aging 27: 576-588. (Pubitemid 43290526)
15. Aberg L, Liewendahl K, Nikkinen P, Autti T, Rinne JO, et al. (2000) Decreased striatal dopamine transporter density in JNCL patients with parkinsonian symptoms. Neurology 54: 1069-1074. (Pubitemid 30151847)
16. Micsenyi MC, Sikora J, Stephney G, Dobrenis K, Walkley SU (2013) Lysosomal membrane permeability stimulates protein aggregate formation in neurons of a lysosomal disease. J Neurosci 33: 10815-10827.
17. Bras J, Verloes A, Schneider SA, Mole SE, Guerreiro RJ (2012) Mutation of the parkinsonism gene ATP13A2 causes neuronal ceroid-lipofuscinosis. Hum Mol Genet 21: 2646-2650.
18. Kettenmann H, Hanisch UK, Noda M, Verkhratsky A (2011) Physiology of microglia. Physiol Rev 91: 461-553.
19. Rose CF, Verkhratsky A, Parpura V (2013) Astrocyte glutamine synthetase: pivotal in health and disease. Biochem Soc Trans 41: 1518-1524.
20. Pontikis CC, Cella CV, Parihar N, Lim MJ, Chakrabarti S, et al. (2004) Late onset neurodegeneration in the Cln32/2 mouse model of juvenile neuronal ceroid lipofuscinosis is preceded by low level glial activation. Brain Res 1023: 231-242. (Pubitemid 39221426)
21. Xiong J, Kielian T (2013) Microglia in Juvenile Neuronal Ceroid Lipofuscinosis (JNCL) are primed towards a proinflammatory phenotype. J Neurochem.
22. Wallraff A, Kohling R, Heinemann U, Theis M, Willecke K, et al. (2006) The impact of astrocytic gap junctional coupling on potassium buffering in the hippocampus. J Neurosci 26: 5438-5447. (Pubitemid 44318396)
23. Takahashi DK, Vargas JR, Wilcox KS (2010) Increased coupling and altered glutamate transport currents in astrocytes following kainic-acid-induced status epilepticus. Neurobiol Dis 40: 573-585.
24. Rouach N, Koulakoff A, Abudara V, Willecke K, Giaume C (2008) Astroglial metabolic networks sustain hippocampal synaptic transmission. Science 322: 1551-1555.
25. Eugenin EA, Basilio D, Saez JC, Orellana JA, Raine CS, et al. (2012) The role of gap junction channels during physiologic and pathologic conditions of the human central nervous system. J Neuroimmune Pharmacol 7: 499-518.
26. Kielian T (2008) Glial connexins and gap junctions in CNS inflammation and disease. J Neurochem 106: 1000-1016.
27. Scemes E, Spray DC, Meda P (2009) Connexins, pannexins, innexins: novel roles of "hemi-channels". Pflugers Arch 457: 1207-1226.
28. Shestopalov VI, Panchin Y (2008) Pannexins and gap junction protein diversity. Cell Mol Life Sci 65: 376-394.
29. Giaume C, Theis M (2009) Pharmacological and genetic approaches to study connexin-mediated channels in glial cells of the central nervous system. Brain Res Rev.
30. Spray DC, Ye ZC, Ransom BR (2006) Functional connexin "hemichannels": a critical appraisal. Glia 54: 758-773. (Pubitemid 44629638)
31. Bennett MV, Contreras JE, Bukauskas FF, Saez JC (2003) New roles for astrocytes: gap junction hemichannels have something to communicate. Trends Neurosci 26: 610-617. (Pubitemid 37338369)
32. Ransom B, Behar T, Nedergaard M (2003) New roles for astrocytes (stars at last). Trends Neurosci 26: 520-522. (Pubitemid 37176905)
33. Ransom BR (2000) Glial modulation of neural excitability mediated by extracellular pH: a hypothesis revisited. Prog Brain Res 125: 217-228. (Pubitemid 35460800)
34. Anderson CM, Swanson RA (2000) Astrocyte glutamate transport: review of properties, regulation, and physiological functions. Glia 32: 1-14.
35. Haydon PG (2001) GLIA: listening and talking to the synapse. Nat Rev Neurosci 2: 185-193. (Pubitemid 33673371)
36. Volterra A, Meldolesi J (2005) Astrocytes, from brain glue to communication elements: the revolution continues. Nat Rev Neurosci 6: 626-640. (Pubitemid 41059337)
37. Takano T, Tian GF, Peng W, Lou N, Libionka W, et al. (2006) Astrocytemediated control of cerebral blood flow. Nat Neurosci 9: 260-267. (Pubitemid 43164550)
38. Mulligan SJ, MacVicar BA (2004) Calcium transients in astrocyte endfeet cause cerebrovascular constrictions. Nature 431: 195-199. (Pubitemid 39243473)
39. Boustany RM (2013) Lysosomal storage diseases-the horizon expands. Nat Rev Neurol 9: 583-598.
40. Mink JW, Augustine EF, Adams HR, Marshall FJ, Kwon JM (2013) Classification and natural history of the neuronal ceroid lipofuscinoses. J Child Neurol 28: 1101-1105.
41. Karpuk N, Burkovetskaya M, Fritz T, Angle A, Kielian T (2011) Neuroinflammation leads to region-dependent alterations in astrocyte gap junction communication and hemichannel activity. J Neurosci 31: 414-425.
42. Orellana JA, Shoji KF, Abudara V, Ezan P, Amigou E, et al. (2011) Amyloid beta-induced death in neurons involves glial and neuronal hemichannels. J Neurosci 31: 4962-4977.
43. Orellana JA, Saez JC, Bennett MV, Berman JW, Morgello S, et al. (2013) HIV increases the release of dickkopf-1 protein from human astrocytes by a Cx43 hemichannel-dependent mechanism. J Neurochem.
44. Groh J, Kuhl TG, Ip CW, Nelvagal HR, Sri S, et al. (2013) Immune cells perturb axons and impair neuronal survival in a mouse model of infantile neuronal ceroid lipofuscinosis. Brain 136: 1083-1101.
45. Qiao X, Lu JY, Hofmann SL (2007) Gene expression profiling in a mouse model of infantile neuronal ceroid lipofuscinosis reveals upregulation of immediate early genes and mediators of the inflammatory response. BMC Neurosci 8: 95.
46. Macauley SL, Pekny M, Sands MS (2011) The role of attenuated astrocyte activation in infantile neuronal ceroid lipofuscinosis. J Neurosci 31: 15575-15585.
47. Jalanko A, Vesa J, Manninen T, von Schantz C, Minye H, et al. (2005) Mice with Ppt1Deltaex4 mutation replicate the INCL phenotype and show an inflammation-associated loss of interneurons. Neurobiol Dis 18: 226-241. (Pubitemid 40092912)
48. Nimmerjahn A, Kirchhoff F, Kerr JN, Helmchen F (2004) Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo. Nat Methods 1: 31-37.
49. Tauskela JS, Hewitt K, Kang LP, Comas T, Gendron T, et al. (2000) Evaluation of glutathione-sensitive fluorescent dyes in cortical culture. Glia 30: 329-341. (Pubitemid 30334334)
50. Sebastia J, Cristofol R, Martin M, Rodriguez-Farre E, Sanfeliu C (2003) Evaluation of fluorescent dyes for measuring intracellular glutathione content in primary cultures of human neurons and neuroblastoma SH-SY5Y. Cytometry A 51: 16-25. (Pubitemid 37517307)
51. Dringen R, Hirrlinger J (2003) Glutathione pathways in the brain. Biol Chem 384: 505-516. (Pubitemid 36609167)
52. Cotman SL, Vrbanac V, Lebel LA, Lee RL, Johnson KA, et al. (2002) Cln3(Deltaex7/8) knock-in mice with the common JNCL mutation exhibit progressive neurologic disease that begins before birth. Hum Mol Genet 11: 2709-2721. (Pubitemid 35214898)
53. Kovacs AD, Saje A, Wong A, Ramji S, Cooper JD, et al. (2012) Age-dependent therapeutic effect of memantine in a mouse model of juvenile Batten disease. Neuropharmacology 63: 769-775.
54. Finn R, Kovacs AD, Pearce DA (2011) Altered sensitivity of cerebellar granule cells to glutamate receptor overactivation in the Cln3(Deltaex7/8)- knock-in mouse model of juvenile neuronal ceroid lipofuscinosis. Neurochem Int 58: 648-655.
55. Kovacs AD, Saje A, Wong A, Szenasi G, Kiricsi P, et al. (2011) Temporary inhibition of AMPA receptors induces a prolonged improvement of motor performance in a mouse model of juvenile Batten disease. Neuropharmacology 60: 405-409.
56. Taylor RM, Farrow BR (1988) Ceroid-lipofuscinosis in border collie dogs. Acta Neuropathol 75: 627-631.
57. Weissenbock H, Rossel C (1997) Neuronal ceroid-lipofuscinosis in a domestic cat: clinical, morphological and immunohistochemical findings. J Comp Pathol 117: 17-24. (Pubitemid 27359047)
58. Oliveira VC, Carrara RC, Simoes DL, Saggioro FP, Carlotti CG, Jr., et al. (2010) Sudan Black B treatment reduces autofluorescence and improves resolution of in situ hybridization specific fluorescent signals of brain sections. Histol Histopathol 25: 1017-1024.
59. Salek RM, Pears MR, Cooper JD, Mitchison HM, Pearce DA, et al. (2011) A metabolomic comparison of mouse models of the Neuronal Ceroid Lipofuscinoses. J Biomol NMR 49: 175-184.
60. Brockmann K, Pouwels PJ, Christen HJ, Frahm J, Hanefeld F (1996) Localized proton magnetic resonance spectroscopy of cerebral metabolic disturbances in children with neuronal ceroid lipofuscinosis. Neuropediatrics 27: 242-248. (Pubitemid 26402550)
61. Pears MR, Cooper JD, Mitchison HM, Mortishire-Smith RJ, Pearce DA, et al. (2005) High resolution 1H NMR-based metabolomics indicates a neurotransmitter cycling deficit in cerebral tissue from a mouse model of Batten disease. J Biol Chem 280: 42508-42514. (Pubitemid 43049207)
62. Eugenin EA, Eckardt D, Theis M, Willecke K, Bennett MV, et al. (2001) Microglia at brain stab wounds express connexin 43 and in vitro form functional gap junctions after treatment with interferon-gamma and tumor necrosis factoralpha. Proc Natl Acad Sci U S A 98: 4190-4195. (Pubitemid 32249920)
63. Garg S, Md Syed M, Kielian T (2005) Staphylococcus aureus-derived peptidoglycan induces Cx43 expression and functional gap junction intercellular communication in microglia. J Neurochem 95: 475-483. (Pubitemid 41457516)
64. Nagasawa K, Chiba H, Fujita H, Kojima T, Saito T, et al. (2006) Possible involvement of gap junctions in the barrier function of tight junctions of brain and lung endothelial cells. J Cell Physiol 208: 123-132. (Pubitemid 43848996)
65. Moriyama Y, Takagi N, Itokawa C, Tanonaka K (2013) Injection of neural progenitor cells attenuates decrease in level of connexin 43 in brain capillaries after cerebral ischemia. Neurosci Lett 543: 152-156.
66. Li AF, Sato T, Haimovici R, Okamoto T, Roy S (2003) High glucose alters connexin 43 expression and gap junction intercellular communication activity in retinal pericytes. Invest Ophthalmol Vis Sci 44: 5376-5382. (Pubitemid 37475413)
67. Corns LF, Deuchars J, Deuchars SA (2013) GABAergic responses of mammalian ependymal cells in the central canal neurogenic niche of the postnatal spinal cord. Neurosci Lett 553: 57-62.
68. Takeuchi H, Mizoguchi H, Doi Y, Jin S, Noda M, et al. (2011) Blockade of gap junction hemichannel suppresses disease progression in mouse models of amyotrophic lateral sclerosis and Alzheimer's disease. PLoS One 6: e21108.
69. Pautler RG (2004) Mouse MRI: concepts and applications in physiology. Physiology (Bethesda) 19: 168-175. (Pubitemid 39481931)
70. Chatziioannou AF (2005) Instrumentation for molecular imaging in preclinical research: Micro-PET and Micro-SPECT. Proc Am Thorac Soc 2: 533-536, 510-511. (Pubitemid 43128025)
71. Valenzuela MJ, Sachdev P (2001) Magnetic resonance spectroscopy in AD. Neurology 56: 592-598. (Pubitemid 32209990)
72. Kuhl TG, Dihanich S, Wong AM, Cooper JD (2013) Regional brain atrophy in mouse models of neuronal ceroid lipofuscinosis: a new rostrocaudal perspective. J Child Neurol 28: 1117-1122.
73. Orellana JA, Figueroa XF, Sanchez HA, Contreras-Duarte S, Velarde V, et al. (2011) Hemichannels in the Neurovascular Unit and White Matter Under Normal and Inflamed Conditions. CNS Neurol Disord Drug Targets.
74. Tsai G, Coyle JT (1995) N-acetylaspartate in neuropsychiatric disorders. Prog Neurobiol 46: 531-540.
75. Tecedor L, Stein CS, Schultz ML, Farwanah H, Sandhoff K, et al. (2013) CLN3 Loss Disturbs Membrane Microdomain Properties and Protein Transport in Brain Endothelial Cells. J Neurosci 33: 18065-18079.
76. Fossale E, Wolf P, Espinola JA, Lubicz-Nawrocka T, Teed AM, et al. (2004) Membrane trafficking and mitochondrial abnormalities precede subunit c deposition in a cerebellar cell model of juvenile neuronal ceroid lipofuscinosis. BMC Neurosci 5: 57.
77. Wolfe DM, Padilla-Lopez S, Vitiello SP, Pearce DA (2011) pH-dependent localization of Btn1p in the yeast model for Batten disease. Dis Model Mech 4: 120-125.
78. Tovar KR, Maher BJ, Westbrook GL (2009) Direct actions of carbenoxolone on synaptic transmission and neuronal membrane properties. J Neurophysiol 102: 974-978.
79. Bramley JR, Wiles EM, Sollars PJ, Pickard GE (2011) Carbenoxolone blocks the light-evoked rise in intracellular calcium in isolated melanopsin ganglion cell photoreceptors. PLoS One 6: e22721.
80. Rouach N, Segal M, Koulakoff A, Giaume C, Avignone E (2003) Carbenoxolone blockade of neuronal network activity in culture is not mediated by an action on gap junctions. J Physiol 553: 729-745. (Pubitemid 38035618)
81. Bastiaanse EM, Jongsma HJ, van der Laarse A, Takens-Kwak BR (1993) Heptanol-induced decrease in cardiac gap junctional conductance is mediated by a decrease in the fluidity of membranous cholesterol-rich domains. J Membr Biol 136: 135-145. (Pubitemid 23353235)
82. Locke D, Harris AL (2009) Connexin channels and phospholipids: association and modulation. BMC Biol 7: 52.
83. Nagy JI, Lynn BD, Tress O, Willecke K, Rash JE (2011) Connexin26 expression in brain parenchymal cells demonstrated by targeted connexin ablation in transgenic mice. Eur J Neurosci 34: 263-271.
84. Iglesias R, Dahl G, Qiu F, Spray DC, Scemes E (2009) Pannexin 1: the molecular substrate of astrocyte "hemichannels". J Neurosci 29: 7092-7097.
85. Scemes E, Suadicani SO, Dahl G, Spray DC (2007) Connexin and pannexin mediated cell-cell communication. Neuron Glia Biol 3: 199-208. (Pubitemid 351594228)
86. Munroe PB, Mitchison HM, O'Rawe AM, Anderson JW, Boustany RM, et al. (1997) Spectrum of mutations in the Batten disease gene, CLN3. Am J Hum Genet 61: 310-316. (Pubitemid 27382306)
87. Herrmann P, Druckrey-Fiskaaen C, Kouznetsova E, Heinitz K, Bigl M, et al. (2008) Developmental impairments of select neurotransmitter systems in brains of Cln3(Deltaex7/8) knock-in mice, an animal model of juvenile neuronal ceroid lipofuscinosis. J Neurosci Res 86: 1857-1870. (Pubitemid 351859435)
88. Zhuo L, Sun B, Zhang CL, Fine A, Chiu SY, et al. (1997) Live astrocytes visualized by green fluorescent protein in transgenic mice. Dev Biol 187: 36-42. (Pubitemid 27359423)
89. Miyasaka N, Takahashi K, Hetherington HP (2006) Fully automated shim mapping method for spectroscopic imaging of the mouse brain at 9.4 T. Magn Reson Med 55: 198-202. (Pubitemid 43062944)
90. Ratiney H, Coenradie Y, Cavassila S, van Ormondt D, Graveron-Demilly D (2004) Time-domain quantitation of 1H short echo-time signals: background accommodation. MAGMA 16: 284-296. (Pubitemid 39006332)
91. Ratiney H, Sdika M, Coenradie Y, Cavassila S, van Ormondt D, et al. (2005) Time-domain semi-parametric estimation based on a metabolite basis set. NMR Biomed 18: 1-13. (Pubitemid 40347537)
92. Paxinos G, Franklin K.B.J. (2001) The Mouse Brain in Stereotaxic Coordinates. San Diego: Academic Press.
93. Karpuk N, Burkovetskaya M, Kielian T (2012) Neuroinflammation alters voltage-dependent conductance in striatal astrocytes. J Neurophysiol 108: 112-123.
94. Esen N, Shuffield D, Syed MM, Kielian T (2007) Modulation of connexin expression and gap junction communication in astrocytes by the gram-positive bacterium S. aureus. Glia 55: 104-117. (Pubitemid 44845513)